Abstract
The unitary firing fields of hippocampal place cells are commonly assumed to be generated by input from entorhinal grid cell modules with differing spatial scales. Here, we review recent research that brings this assumption into doubt. Instead, we propose that place cell spatial firing patterns are determined by environmental sensory inputs, including those representing the distance and direction to environmental boundaries, while grid cells provide a complementary self-motion related input that contributes to maintaining place cell firing. In this view, grid and place cell firing patterns are not successive stages of a processing hierarchy, but complementary and interacting representations that work in combination to support the reliable coding of large-scale space.
Highlights
Modulated firing in the hippocampal formation The medial temporal lobes, and hippocampus in particular, have long been implicated in episodic and spatial memory function in humans and animals respectively [1,2,3]
Following the discovery of grid cells, several theoretical studies established that place fields could be generated by combining grid firing patterns with different spatial scales [13,14,15,16,17,18,19,20,21,22,23,24], and grid cell input has subsequently come to be considered the primary determinant of place cell firing (e.g., [25])
Place cells are present throughout the dorsoventral axis of the hippocampus, but place fields are larger towards the ventral pole [37,38,39]
Summary
In addition to place and grid cells, the hippocampal formation contains several other spatially modulated cell types, including head direction cells [5,6,7], boundary cells [9,10,11,12], and cells that encode object locations [99,100]. Boundary cells of the subiculum [9,10], parasubiculum [11], and mEC [11,12] fire whenever a boundary is at a particular distance and direction from the current location of the animal, independent of head direction, and exhibit a second firing field at the same distance and direction to additional boundaries placed within a familiar environment (Figure 1C) [9,10,11] These cells maintain their firing patterns in darkness and rotate with polarising visual stimuli, coherently with head direction and grid cells [10,11]. CA1 sends output projections to the deeper layers of EC, both directly and via the subiculum; the subiculum sends output projections to pre- and parasubiculum; and there are tentative reports of a back-projection from subiculum to CA1, it is not clear if this is excitatory or inhibitory in nature [60,61,103,104]
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